Burton was returned to the Assembly in a 1988 special election to succeed Art Agnos, who had been elected Mayor of San Francisco. Burton also served in the U.S. House of Representatives, alongside his brother, from 1975-82, when he resigned. As a legislator, Burton was known for expanding the Cal Grant scholarship program, and passing a law (subsequently defeated in a referendum) that would have required California businesses to pay for health coverage for their workers. The magazine California Journal said about Burton's departure from the Senate in 2005: "Gone will be the Senate's most vehement partisan for social services for the poor, the Senate's angriest voice against tax breaks for businesses and the wealthy, its loudest voice for protection of workers, its fiercest pro-labor advocate and its disciplinarian."[1]

After leaving the Senate, Burton formed the John Burton Foundation, an organization that, according to its web site, is "dedicated to improving the quality of life for California’s homeless children and developing policy solutions to prevent homelessness." In February 2007 he was appointed board member of the University of Phoenix.[2]

In 2008, Burton settled a $10 million sexual harassment lawsuit filed by Kathleen Driscoll, then the executive director of his charitable foundation for homeless children. She claimed Burton sexually harassed her by making unwanted advances, using suggestive language and commenting on her body.

At a 2008 news conference in her attorney's office, Driscoll said, "I had a dream of helping homeless children through a job I loved. John Burton turned that dream into a sexual harassment nightmare and quite frankly a living hell." [5]